Letter | Published:

Neurocranial development of the coelacanth and the evolution of the sarcopterygian head

Nature (2019) | Download Citation

Abstract

The neurocranium of sarcopterygian fishes was originally divided into an anterior (ethmosphenoid) and posterior (otoccipital) portion by an intracranial joint, and underwent major changes in its overall geometry before fusing into a single unit in lungfishes and early tetrapods1. Although the pattern of these changes is well-documented, the developmental mechanisms that underpin variation in the form of the neurocranium and its associated soft tissues during the evolution of sarcopterygian fishes remain poorly understood. The coelacanth Latimeria is the only known living vertebrate that retains an intracranial joint2,3. Despite its importance for understanding neurocranial evolution, the development of the neurocranium of this ovoviviparous fish remains unknown. Here we investigate the ontogeny of the neurocranium and brain in Latimeria chalumnae using conventional and synchrotron X-ray micro-computed tomography as well as magnetic resonance imaging, performed on an extensive growth series for this species. We describe the neurocranium at the earliest developmental stage known for Latimeria, as well as the major changes that the neurocranium undergoes during ontogeny. Changes in the neurocranium are associated with an extreme reduction in the relative size of the brain along with an enlargement of the notochord. The development of the notochord appears to have a major effect on the surrounding cranial components, and might underpin the formation of the intracranial joint. Our results shed light on the interplay between the neurocranium and its adjacent soft tissues during development in Latimeria, and provide insights into the developmental mechanisms that are likely to have underpinned the evolution of neurocranial diversity in sarcopterygian fishes.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Data availability

The PPC-SRμCT acquisitions are available online at http://paleo.esrf.eu. All surface files are deposited online at http://phenome10k.org. Any other relevant data are available from the corresponding author upon reasonable request.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Ahlberg, P. E., Clack, J. A. & Luksevics, E. Rapid braincase evolution between Panderichthys and the earliest tetrapods. Nature 381, 61–64 (1996).

  2. 2.

    Anthony, J. & Robineau, D. Sur quelques caractères juvéniles de Latimeria chalumnae Smith (Pisces, Crossopterygii Coelacanthidae). C. R. Acad. Sci. Ser. D 283, 1739–1742 (1976).

  3. 3.

    Millot, J. & Anthony, J. Anatomie de Latimeria chalumnae. II. Système Nerveux et Organes des Sens (Centre National de la Recherche Scientifique, Paris, 1965).

  4. 4.

    Smith, J. L. B. A living fish of the Mesozoic type. Nature 143, 455–456 (1939).

  5. 5.

    Kuratani, S. Development of the chondrocranium of the loggerhead turtle, Caretta caretta. Zool. Sci. 16, 803–818 (1999).

  6. 6.

    de Beer, G. R. The Development Of The Vertebrate Skull (Univ. Chicago Press, Chicago, 1938).

  7. 7.

    Goodrich, E. S. Studies on the Structure and Development of Vertebrates Vol. 1 (Macmillan, London, 1930).

  8. 8.

    Clement, A. M. et al. Neurocranial anatomy of an enigmatic Early Devonian fish sheds light on early osteichthyan evolution. eLife 7, e34349 (2018).

  9. 9.

    Janvier, P. Early Vertebrates (Clarendon, Oxford, 1996).

  10. 10.

    Lu, J. et al. The earliest known stem-tetrapod from the Lower Devonian of China. Nat. Commun. 3, 1160 (2012).

  11. 11.

    Giles, S. & Friedman, M. Virtual reconstruction of endocast anatomy in early ray-finned fishes (Osteichthyes, Actinopterygii). J. Paleontol. 88, 636–651 (2014).

  12. 12.

    Lu, J. et al. A Devonian predatory fish provides insights into the early evolution of modern sarcopterygians. Sci. Adv. 2, e1600154 (2016).

  13. 13.

    Yu, X. A new porolepiform-like fish, Psarolepis romeri, gen. et sp. nov. (Sarcopterygii, Osteichthyes) from the Lower Devonian of Yunnan, China. J. Vertebr. Paleontol. 18, 261–274 (1998).

  14. 14.

    Andrews, S. M., Long, J. A., Ahlberg, P. E., Barwick, R. E. & Campbell, K. The structure of the sarcopterygian Onychodus jandemarrai n. sp. from Gogo, Western Australia: with a functional interpretation of the skeleton. Trans. R. Soc. Edinb. Earth Sci. 96, 197–307 (2006).

  15. 15.

    Kuratani, S., Adachi, N., Wada, N., Oisi, Y. & Sugahara, F. Developmental and evolutionary significance of the mandibular arch and prechordal/premandibular cranium in vertebrates: revising the heterotopy scenario of gnathostome jaw evolution. J. Anat. 222, 41–55 (2013).

  16. 16.

    Kuratani, S. The neural crest and origin of the neurocranium in vertebrates. Genesis 56, e23213 (2018).

  17. 17.

    Clack, J. A. in Major Events in Early Vertebrate Evolution (Systematics Association Special Volume Series 61) (ed. Ahlberg, P. E.) 392–505 (Taylor and Francis, London, 2001).

  18. 18.

    Kemp, A. Ontogeny of the skull of the Australian lungfish Neoceratodus forsteri (Osteichthyes: Dipnoi). J. Zool. (Lond.) 248, 97–137 (1999).

  19. 19.

    Nieuwenhuys, R. et al. (eds) The Central Nervous System of Vertebrates Vols 1–3 (Springer, Berlin, Germany, 1998).

  20. 20.

    Maisey, J. G. in Major Events in Early Vertebrate Evolution (Systematics Association Special Volume Series 61) (ed. Ahlberg, P. E.) 263–288 (Taylor and Francis, London, 2001).

  21. 21.

    Kemp, A. Early development of neural tissues and mesenchyme in the Australian lungfish Neoceratodus forsteri (Osteichthyes: Dipnoi). J. Zool. (Lond.) 250, 347–372 (2000).

  22. 22.

    Ahlberg, P. E., Clack, J. A., Lukševičs, E., Blom, H. & Zupiņs, I. Ventastega curonica and the origin of tetrapod morphology. Nature 453, 1199–1204 (2008).

  23. 23.

    Mee-Mann, C. The Braincase of Youngolepis, a Lower Devonian Crossopterygian from Yunnan, South-Western China. PhD thesis, Univ. Stockholm and Swedish Museum of Natural History (1982).

  24. 24.

    Pradel, A. et al. Skull and brain of a 300-million-year-old chimaeroid fish revealed by synchrotron holotomography. Proc. Natl Acad. Sci. USA 106, 5224–5228 (2009).

  25. 25.

    Kruska, D. C. T. The brain of the basking shark (Cetorhinus maximus). Brain Behav. Evol. 32, 353–363 (1988).

  26. 26.

    Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P. E. A primitive placoderm sheds light on the origin of the jawed vertebrate face. Nature 507, 500–503 (2014).

  27. 27.

    Clement, A. M., Nysjö, J., Strand, R. & Ahlberg, P. E. Brain–endocast relationship in the Australian lungfish, Neoceratodus forsteri, elucidated from tomographic data (Sarcopterygii: Dipnoi). PLoS ONE 10, e0141277 (2015).

  28. 28.

    Northcutt, R. G., Neary, T. J. & Senn, D. G. Observations on the brain of the coelacanth Latimeria chalumnae: external anatomy and quantitative analysis. J. Morphol. 155, 181–192 (1978).

  29. 29.

    Clement, A. M. & Ahlberg, P. E. The first virtual cranial endocast of a lungfish (Sarcopterygii: Dipnoi). PLoS ONE 9, e113898 (2014).

  30. 30.

    Dutel, H., Herbin, M., Clément, G. & Herrel, A. Bite force in the extant coelacanth Latimeria: the role of the intracranial joint and the basicranial muscle. Curr. Biol. 25, 1228–1233 (2015).

  31. 31.

    Nulens, R., Scott, L. & Herbin, M. An Updated Inventory of All Known Specimens of the Coelacanth Latimeria spp. Smithiana Special Publication 3 (South African Institute for Aquatic Biodiversity, Grahamstown, 2011).

  32. 32.

    Benno, B. et al. Coelacanth (Latimeria chalumnae Smith, 1939) discoveries and conservation in Tanzania. S. Afr. J. Sci. 102, 486–490 (2006).

  33. 33.

    Hureau, J.-C. & Ozouf, C. Détermination de l’âge et croissance du coelacanthe Latimeria chalumnae Smith, 1939 (Poisson. Crossopterygien, Coelacanthidé). Cybium 2, 129–137 (1977).

  34. 34.

    Dutel, H., Herrel, A., Clément, G. & Herbin, M. A reevaluation of the anatomy of the jaw-closing system in the extant coelacanth Latimeria chalumnae. Naturwissenschaften 100, 1007–1022 (2013).

  35. 35.

    Dutel, H., Herrel, A., Clément, G. & Herbin, M. Redescription of the hyoid apparatus and associated musculature in the extant coelacanth Latimeria chalumnae: functional implications for feeding. Anat. Rec. 298, 579–601 (2015).

Download references

Acknowledgements

We thank R. Bills and A. Paterson (South African Institute for Aquatic Biodiversity (SAIAB)) for the loan of the fetus; and D. Neumann (Zoologische Staatssammlung München (ZSM)) for the loan of P2; M. Garcia Sanz for micro-computed tomography scanning of the adult specimen at ‘AST-RX, plate-forme d’accès scientifique à la tomographie à rayons X’ in the ‘UMS 2700 Outils et Méthodes de Systématique intégrative CNRS-MNHN’; the European Synchrotron Radiation Facility (ESRF) for granting beam time to H.D. on ID19 for performing the PPC-SRμCT acquisitions (Proposal EC-1023); C. Bens and A. Verguin of the Collections de Pièces anatomiques en Fluides at the Muséum National d’Histoire Naturelle (MNHN) for their help; and É. Heude (MNHN) and P. Gueriau (University of Lausanne) for their comments and input on an earlier version of the draft. This work was supported by a grant from Agence Nationale de la Recherche under the LabEx ANR-10-LABX-0003-BCDiv, in the program ‘Investissements d’avenir’ n\u0001 ANR-11-IDEX-0004-02. H.D. was supported by a BBSRC grant (BB/M008525/1).

Reviewer information

Nature thanks Per Ahlberg and Matt Friedman for their contribution to the peer review of this work.

Author information

Affiliations

  1. School of Engineering and Computer Science, Medical and Biological Engineering Research Group, University of Hull, Hull, UK

    • Hugo Dutel
    •  & Michael J. Fagan
  2. School of Earth Sciences, University of Bristol, Bristol, UK

    • Hugo Dutel
  3. UMR 7206 (MNHN-CNRS-Université Paris Diderot), Éco-Anthropologie et Ethnobiologie, Département Homme et Environnement, Muséum National d’Histoire Naturelle, Paris, France

    • Manon Galland
  4. European Synchrotron Radiation Facility, Grenoble, France

    • Paul Tafforeau
  5. College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia

    • John A. Long
  6. UMR 7207 (MNHN-CNRS-Sorbonne Université), CR2P Centre de Recherche en Paléontologie-Paris, Département Origines et Évolution, Muséum National d’Histoire Naturelle, Paris, France

    • Philippe Janvier
    •  & Gaël Clément
  7. UMR 7179 (MNHN-CNRS) MECADEV, Département Adaptations du Vivant, Muséum National d’Histoire Naturelle, Paris, France

    • Anthony Herrel
    •  & Marc Herbin
  8. Inserm U 1127, CNRS UMR 7225, Centre for NeuroImaging Research, ICM (Brain & Spine Institute), Sorbonne University, Paris, France

    • Mathieu D. Santin

Authors

  1. Search for Hugo Dutel in:

  2. Search for Manon Galland in:

  3. Search for Paul Tafforeau in:

  4. Search for John A. Long in:

  5. Search for Michael J. Fagan in:

  6. Search for Philippe Janvier in:

  7. Search for Anthony Herrel in:

  8. Search for Mathieu D. Santin in:

  9. Search for Gaël Clément in:

  10. Search for Marc Herbin in:

Contributions

H.D., G.C., M.H., A.H. and P.J. designed the research. H.D. and P.T. made the PPC-SRμCT acquisitions. H.D., G.C. and M.H. made the conventional microtomographical acquisitions with the assistance of local staff. M.D.S. made the magnetic resonance imaging acquisitions. H.D. segmented the scans and made the three-dimensional rendering of all of the developmental stages, with the assistance of M.G. J.A.L. provided fossil material for comparative study and provided input for the discussion. M.J.F. and A.H. provided input for the results and discussion. H.D. wrote the manuscript, and made the figures and scientific illustrations. All other authors provided critical comments and were involved in the writing of the manuscript. All authors accepted the final version of the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Hugo Dutel.

Extended data figures and tables

  1. Extended Data Fig. 1 The neurocranium of the fetus of L. chalumnae.

    a, b, The neurocranium in right anterolateral view, with the ethmosphenoid portion virtually cut open along the mid-sagittal plane in b. c, d, Dorsal view of the neurocranium with the roof of the otoccipital portion virtually cut open. The brain is shown in position in c, and was digitally removed in d to show the underlying neurocranial structures. e, Posterior view of the ethmosphenoid portion. f, Posterior view of the otoccipital portion.

  2. Extended Data Fig. 2 Comparison of the neurocranium between the fetus and P1 of L. chalumnae.

    Coronal sections obtained from PPC-SRμCT acquisition along the head of the fetus (left column) and P1 (right column) of L. chalumnae. a, Section at the level of the orbital foramen. b, Section at the level of the hypophyseal fossa. c, Section at the level of the basisphenoid–palatoquadrate joint. d, Section at the level of the inner ear. Sample size for each stage, n = 1.

  3. Extended Data Fig. 3 Endocranium and brain morphology in L. chalumnae growth series.

    ae, The fetus (a), P1 (b), P2 (c), juvenile (d) and adult (e) in right lateral (left) and dorsal (right) views. Grey portions in the juvenile (d) were reconstructed based on P2 (c). The rostral organ was not reconstructed in d, because it had been destroyed in the dissection of this specimen. IX, glossopharyngeal nerve. Sample size for each stage, n = 1.

  4. Extended Data Fig. 4 The brain of L. chalumnae at different stages of development.

    ad, The brains of the fetus (a), P1 (b), P2 (c) and adult (d) are shown in right lateral view (left) and dorsal (right) views. The brain of the juvenile is not displayed, because it was extracted from the endocranium and was not imaged in situ. Sample size for each stage, n = 1.

  5. Extended Data Fig. 5 The brain of the juvenile in situ.

    Photograph taken during the dissection of the juvenile (MNHN C79 (CCC 94)) in 1974 at the MNHN. As in earlier developmental stages, the brain spans the intracranial joint (indicated by the needle) in the juvenile. Scale in centimetres.

  6. Extended Data Table 1 Morphometric measurements of the notochord, brain and endocranial cavity
  7. Extended Data Table 2 Protocols of the PPC-SRμCT acquisitions

Supplementary information

  1. Supplementary Information

    Supplementary Information contains Supplementary Results and Discussion, and additional references

  2. Reporting Summary

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41586-019-1117-3

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.